SERCA1 expression enhances the metabolic efficiency of improved contractility in post-ischemic heart

Journal of Molecular and Cellular Cardiology

Volumn 47, Issue 5, 2009, Pages 614-621

  O'Donnell, J Michael ^a   Pound, Kayla ^a   Xu, Xianyao ^a   Lewandowski, E Douglas ^a  

^a Program in Integrative Cardiac Metabolism   (United States)

Author keywords

Fatty acid oxidation; Metabolism; PCr ATP; Reperfusion; SERCA

Indexed keywords

ADENOSINE TRIPHOSPHATE; COMPLEMENTARY DNA; CREATINE PHOSPHATE; FATTY ACID; GLUCOSE; PALMITIC ACID; PHOSPHATE BUFFERED SALINE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; TRICARBOXYLIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; CITRIC ACID CYCLE; CONTROLLED STUDY; CORONARY ARTERY BLOOD FLOW; FATTY ACID OXIDATION; GENE OVEREXPRESSION; GENE TRANSFER; HEART FUNCTION; HEART LEFT VENTRICLE DP-DT; HEART MUSCLE CONTRACTILITY; HEART MUSCLE ISCHEMIA; HEART MUSCLE REPERFUSION; HEART PERFUSION; HEART WORK; IN VIVO STUDY; ISOLATED HEART; MALE; MITOCHONDRION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPRAGUE DAWLEY RAT; STUNNED HEART MUSCLE;

ADENOSINE TRIPHOSPHATE; ANIMALS; ENERGY METABOLISM; HEART; KINETICS; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MITOCHONDRIA, HEART; MODELS, BIOLOGICAL; MYOCARDIAL REPERFUSION INJURY; MYOCARDIAL STUNNING; MYOCARDIUM; OXIDATION-REDUCTION; PALMITATES; PHOSPHOCREATINE; RATS; RATS, SPRAGUE-DAWLEY; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES;

ADENOVIRIDAE; RATTUS;

EID: 70349884021     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2009.08.031     Document Type: Article

References (41)

1. Talukder M.A.H., Kalyanasundaram A., Zhao X., Zuo L., Bhupathy P., Babu G.J., et al. Expression of SERCA isoform with faster Ca2+ transport properties improves postischemic cardiac function and Ca2+ handling and decreases myocardial infarction. Am. J. Physiol. Heart Circ. Physiol. 293 (2007) H2418-H2428
2. Chen Y., Escoubet B., Prunier F., Amour J., Simonides W.S., Vivien B., et al. Constitutive cardiac overexpression of sarcoplasmic/endoplasmic reticulum Ca2+-ATPase delays myocardial failure after myocardial infarction in rats at a cost of increased acute arrhythmias. Circulation 109 (2004) 1898-1903
3. Periasamy M., and Huke S. SERCA pump level is a critical determinant of Ca2+ homeostasis and cardiac contractility. J. Mol. Cell. Cardiol. 33 (2001) 1053-1063
4. Del Monte F., Lebeche D., Guerrero J.L., Tsuji T., Doye A.A., Gwathmey J.K., et al. Abrogation of ventricular arrhythmias in a model of ischemia and reperfusion by targeting myocardial calcium cycling. Proc. Natl. Acad. Sci. 101 (2004) 5622-5627
5. McCormack J.G., Halestrap A.P., and Denton R.M. Role of calcium ions in regulation of mammalian intramitochondrial metabolism. Physiol. Rev. 70 (1990) 391-417
6. Wan B., LaNoue K.F., Cheung J.Y., and Scaduto Jr. R.C. Regulation of citric acid cycle by calcium. J. Biol. Chem. 264 (1989) 13430-13439
7. Balaban R.S. Cardiac energy metabolism homeostasis: role of cytosolic calcium. J. Mol. Cell. Cardiol. 34 (2002) 1259-1271
8. Laster S.B., Becker L.C., Ambrosio G., and Jacobus W.E. Reduced aerobic metabolic efficiency in globally "stunned" myocardium. J. Mol. Cell. Cardiol. 21 (1989) 419-426
9. Lewandowski E.D., Yu X., LaNoue K.F., White L.T., Doumen C., and O'Donnell J.M. Altered metabolite exchange between subcellular compartments in intact postischemic rabbit hearts. Circ. Res. 81 (1997) 165-175
10. Liu B., elAlaoui-Talibi Z., Clanachan A.S., Schulz R., and Lopaschuk G.D. Uncoupling of contractile function from mitochondrial TCA cycle activity and MVO2 during reperfusion of ischemic hearts. Am. J. Physiol. Heart Circ. Physiol. 270 39 (1996) H72-H80
11. Weiss R.G., Kalil-Filho R., Herskowitz A., Chacko V.P., and Litt M. Tricarboxylic acid cycle activity in postischemic rat hearts. Circulation 87 (1993) 270-282
12. Lewandowski E.D., and Johnston D.L. Reduced substrate oxidation in postischemic myocardium 13C and 31P NMR analyses. Am. J. Physiol. Heart. Circ. Physiol. 2598 27 (1990) H1357-H1365
13. O'Donnell J.M., White L.T., and Lewandowski E.D. Mitochondrial transporter responsiveness and metabolic flux homeostasis in postischemic hearts. Am. J. Physiol. 277 (1999) H866-H873
14. LaNoue D.F., and Williamson J.R. Interrelationships between malate-aspartate shuttle and citric acid cycle in rat heart mitochondrial. Metabolism 20 (1992) 119-140
15. O'Donnell J.M., Doumen C., LaNoue K.F., White L.T., Yu X., Alpert N.M., et al. Dehydrogenase regulation of metabolite oxidation and efflux from mitochondria in intact hearts. Am. J. Physiol. 43 (1998) H467-H476
16. Terrand J., Papageorgiou I., Rosenblatt-Velin N., and Lerch R. Calcium-mediated activation of pyruvate dehydrogenase in severely injured postischemic myocardium. Am. J. Physiol. Heart Circ. Physiol. 281 (2001) H722-H730
17. Lewandowski E.D., and White L.T. Pyruvate dehydrogenase influences postischemic heart function. Circulation 91 (1995) 2071-2079
18. Wambolt R.B., Lopaschuk G.D., Brownsey R.W., and Allard M.F. Dichloroacetate improves postischemic function of hypertrophied rat hearts. J. Am. Coll. Cardiol. 36 4 (2000) 1378-1385
19. O'Donnell J.M., and Lewandowski E.D. Efficient, cardiac-specific adenoviral gene transfer by isolated retrograde perfusion in vivo. . 12 (2005) 958-965
20. O'Donnell J.M., and Lewandowski E.D. Controlling specificity and efficiency of adenoviral gene transfer in heart by catheter based coronary perfusion. In: Niewohner, and Tannert (Eds). Gene Therapy - Prospective assessment in its societal context (2006), Elsevier (pub) 33-46
21. O'Donnell J.M., Fields A., Xu X., Chowdhury S.A.K., Geenen D.L., and Bi J. Limited functional and metabolic improvements in hypertrophic and healthy rat heart overexpressing the skeletal muscle isoform of SERCA1 by adenoviral gene transfer in vivo. Am. J. Physiol. Heart Circ. Physiol. 295 (2008) H2483-H2494
22. O'Donnell J.M., Fields A., Sorokina N., and Lewandowski E.D. The absence of endogenous lipid oxidation in early stage heart failure exposes limits in lipid storage and turnover. J. Mol. Cell. Physiol. 44 2 (2008) 315-322
23. O'Donnell J.M., White L.T., Alpert N.M., Griffin J.L., and Lewandowski E.D. Coupling of mitochondrial fatty acid uptake to oxidative flux in the intact heart. Biophys. J. 82 1 (2002 Jan) 11-18
24. Malloy C.R., Sherry A.D., and Jeffrey F.M.H. Evaluation of carbon flux and substrate selection through alternate pathways involving the citric acid cycle of the heart by 13C NMR spectroscopy. J. Biol. Chem. 263 (1989) 6965-6971
25. Yu X., Alpert N.M., and Lewandowski E.D. Modeling enrichment kinetics from dynamic 13C NMR spectra: theoretical analysis and practical considerations. Am. J. Physiol. Cell Physiol. 272 (1997) C2037-C2048
26. Del Monte F., Williams E., Lebeche D., Schmidt U., Rosenzweig A., Gwathmey J.K., et al. Improvement in survival and cardiac metabolism after gene transfer of sarcoplasmic reticulum Ca(2+)-ATPase in a rat model of heart failure. Circulation 104 12 (2001;Sep18) 1424-1429
27. Periasamy M., and Kalyanasundaram A. SERCA pump isoforms: their role in calcium transport and disease. Muscle Nerve 35 (2007) 430-442
28. Cavagna M., O'Donnell J.M., Sumbilla C., Inesi G., and Klein M.G. Exogenous Ca2+-ATPase isoform effects on Ca2+ transients of embryonic chicken and neonatal rat cardiac myocytes. J. Physiol. 528 1 (2000) 53-63
29. Inesi G., Cavagna M., O'Donnell J.M., Sumbilla C., Zhong L., Ma H., et al. Adenovirus mediated gene transfer of SERCA isoforms. In: Hasenfuss G., and Marban E. (Eds). Molecular Approaches to the Therapy of Heart Failure (2000), Springer-Steinkopff, Germany 76-88
30. Logeart D., Vinet L., Ragot T., Heimburger M., Louedec L., Michel J.B., et al. Percutaneous intracoronary delivery of SERCA gene increases myocardial function: a tissue Doppler imaging echocardiographic study. Am. J. Physiol. Heart Circ. Physiol. 291 (2006) H1773-H1779
31. Viner R.I., Ferrington D.A., Willioms T.D., Bigelow D.J., and Schoneich C. Protein modification during biological aging: selective tyrosine nitration of the SERCA2a isoform of the sarcoplasmic reticulum Ca2+-ATPase in skeletal muscle. Biochem. J. 340 (1999) 667-669
32. Wolosker H., Rocha J.B.T., Engelender S., Panizzutti R., Miranda J.D., and de Meis L. Sarco/endoplasmic reticulum Ca2+-ATPase isoforms: diverse responses to acidosis. Biochem. J. 321 (1997) 545-550
33. Vetter R., Rehfeld U., Reissfelder C., Weiss W., Wagner K.D., Gunther J., et al. Transgenic overexpression of the sarcoplasmic reticulum Ca2+ATPase improves reticular Ca2+ handling in normal and diabetic rat hearts. FASEB J. 16 12 (2002; Oct) 1657-1659
34. Huke S., Prasad V., Nieman M.L., Nattamai K.J., Grupp I.L., Lorenz J.N., et al. Altered dose response to β-agonists in SERCA1-expressing hearts ex vivo and in vivo. Am. J. Physiol. Heart Circ. Physiol. 283 (2002) H958-H966
35. He H., Giordano F.J., Hilal-Dandan R., Choi D.J., Rockman H.A., McDonough P.M., et al. Overexpression of the rat sarcoplasmic reticulum Ca2+ ATPase gene in the heart of transgenic mice accelerates calcium transients and cardiac relaxation. J. Clin. Invest. 100 (1997) 380-389
36. O'Donnell J.M., Kudej R.K., White L.T., LaNoue K.F., Vatner S.F., and Lewandowski E.D. Limited transfer of cytosolic NADH into mitochondria at high cardiac workload. Am. J. Physiol. Heart Circ. Physiol. 286 6 (2004) H2237-H2242
37. Dawson A.G. Oxidation of cytosolic NADH formed during aerobic metabolism in mammalian cells. Trends Biochem. Sci. 4 (1979) 171-176
38. Sluse F.E., Goffart G., and Liebecq C. Mechanism of the exchanges catalysed by the oxoglutarate translocator of rat heart mitochondria. Kinetics of the external-product inhibition. Eur. J. Biochem. 32 (1973) 283-291
39. Belke D.D., Swanson E., Suarez J., Scott B.T., Stenbit A.E., and Dillmann W.H. Increased expression of SERCA in the hearts of transgenic mice results in increased oxidation of glucose. Am. J. Physiol. Heart Circ. Physiol. 292 (2007) H1755-H1763
40. Van der Vusse G.J., and van Bilsen M. Free fatty acids and postischemic myocardial function. Sem. Cardiothor. Basc. Anesthesia 10 3 (2006) 231-235
41. Tamm C., Benzi R., Papageorgiou I., Tardy I., and Lerch R. Substrate competition in postischemic myocardium. Effect of substrate availability during reperfusion on metabolic and contractile recovery in isolated rat hearts. Circ. Res. 75 (1994) 1103-1112